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Article Developing an Atlas of Harmful Algal Blooms in the Red : Linkages to Local Aquaculture

Elamurugu Alias Gokul 1, Dionysios E. Raitsos 2 , John A. Gittings 1 and Ibrahim Hoteit 1,* 1 Earth Science and Engineering (ErSE), King Abdullah University of Science and Technology (KAUST), Thuwal 23955, ; [email protected] (E.A.G.); [email protected] (J.A.G.) 2 Department of Biology, National and Kapodistrian University of Athens (NKUA), 15784 Athens, Greece; [email protected] * Correspondence: [email protected]

 Received: 11 September 2020; Accepted: 2 November 2020; Published: 11 November 2020 

Abstract: Harmful algal blooms (HABs) are one of the leading causes of biodiversity loss and alterations to services. The is one of the least studied large marine (LMEs), and knowledge on the large-scale spatiotemporal distribution of HABs remains limited. We implemented the recently developed remote sensing algorithm of Gokul et al. (2019) to produce a high-resolution atlas of HAB events in the Red Sea and investigated their spatiotemporal variability between 2003 and 2017. The atlas revealed that (i) the southern part of the Red Sea is subject to a higher occurrence of HABs, as well as long-lasting and large-scale events, in comparison to the northern part of the basin, and (ii) the Red Sea HABs exhibited a notable seasonality, with most events occurring during summer. We further investigated the potential interactions between identified HAB events and the National Aquaculture Group (NAQUA), Al-Lith (Saudi Arabia)—the largest aquaculture facility on the Red Sea coast. The results suggest that the spatial coverage of HABs and 3 the elevated -a (Chl-a)(> 1 mg m− ; a proxy for high nutrient concentration), in the coastal waters of Al-Lith during summer, increased concurrently with the local aquaculture annual production over a nine-year period (2002–2010). This could be attributed to excessive nutrient loading from the NAQUA facility’s outfall, which enables the proliferation of HABs in an otherwise oligotrophic region during summer. Aquaculture is an expanding, high-value industry in the Kingdom of Saudi Arabia. Thus, a wastewater management plan should ideally be implemented at a national level, in order to prevent excessive nutrient loading. Our results may assist policy-makers’ efforts to ensure the sustainable development of the Red Sea’s coastal economic zone.

Keywords: harmful algal blooms; Red Sea; remote sensing; aquaculture

1. Introduction In global marine ecosystems, harmful algal blooms (HABs) are known for the rapid increase of algal and occasionally the production of toxins [1]. HABs are often associated with a broad range of ecological impacts, including increased mortalities of wild and farmed fish, displacement of indigenous species, and alterations to marine food webs, which ultimately have a detrimental effect on human societies [2,3]. HABs constitute a worldwide issue, which is constantly intensified in its frequency and spatial extent, primarily due to oceanic warming () and increasing anthropogenic pollution [4–7]. The Red Sea, a large (LME) characterized by thriving coral complexes, high levels of biological diversity, and a growing aquaculture industry, is one such region that has been subjected to substantial impacts from HABs [8–17]. A recent study summarized historical HAB events that were previously reported by different field sampling programs in the Red Sea over the last

Remote Sens. 2020, 12, 3695; doi:10.3390/rs12223695 www.mdpi.com/journal/remotesensing Remote Sens. 2020, 12, 3695 2 of 14 three decades [18]. The main functional types (PFTs) responsible for the reported HAB events were found to be dinoflagellates, , and [18–20]. Besides traditional in situ approaches, Gokul et al. [17] developed and validated a remote sensing model to detect and map the spatial distribution of HABs associated with the aforementioned PFTs in the Red Sea. Several studies focusing on Red Sea HABs have enabled a deeper understanding of their spatiotemporal distribution, species toxicity levels (only possible through in situ measurements) and the underlying oceanographic mechanisms responsible for their outbreaks [12,17,18]. For instance, previous studies have conducted field sampling programs and reported several HAB species including Kryptoperidinium foliaceum, /miliaris, Heterosigma akashiwo, var. bahamense, sp. and the cyanobacterium Trichodesmium erythraeum [8–16]. Mohamed [18] documented the main environmental factors contributing to the dominance of these HAB species. Recently, a remote sensing algorithm was developed to investigate the spatial variability of these HAB species in the Red Sea, in accordance with previously reported events in the Red Sea [17]. However, studies on Red Sea HABs are limited with regards to the investigation of their large-scale spatial distribution, long-term temporal (interannual and/or seasonal) evolution, and interactions with local aquaculture industries. Such information is essential for the regional economy (i.e., fisheries, aquaculture, and tourism) and will support policy-makers to optimize the sustainable management of the Red Sea’s coastal economic zone. For instance, the National Aquaculture Group (NAQUA) located at the coastal city Al-Lith is the largest aquaculture facility in the Red Sea and is an important source of food and economic prosperity to the Kingdom of Saudi Arabia. Thus, routine monitoring of HABs over the relevant spatial–temporal scales is required in order to develop a more sustainable aquaculture operation and to improve coastal management strategies [11,20,21]. Here, we implemented the remote sensing algorithm developed by Gokul et al. [17] on a 15-year satellite-derived remote sensing reflectance (Rrs) dataset (2003–2017) to produce an atlas of HAB events in the Red Sea. Furthermore, we investigated the interactions between HAB events and Al-Lith’s NAQUA aquaculture facility. Our HAB Red Sea atlas will assist the policy-makers with regional decision-making and risk mitigation processes that are associated with environmental and aquaculture management.

2. Materials and Methods This study used the recently developed remote sensing algorithm of Gokul et al. [17] to develop an atlas of HABs in the Red Sea and then investigate their possible linkages to the largest aquaculture of the basin. This remote sensing algorithm was developed by applying high resolution satellite-derived Rrs observations and available in situ datasets to a second order derivative technique for detecting the presence/absence and mapping the spatial distribution of HABs in the Red Sea [17].

2.1. Satellite Datasets

Satellite remote sensing datasets of Rrs were acquired from the Moderate Resolution Imaging Spectroradiometer (MODIS) and the Medium Resolution Imaging Spectrometer (MERIS). Satellite-derived observations of Chlorophyll-a concentration (Chl-a) were obtained from the Ocean Colour Climate Change Initiative (OC-CCI) of the European Space Agency (ESA). We obtained MODIS-Aqua and MERIS datasets from the NASA archive (https://oceancolor.gsfc.nasa.gov), whereas the OC-CCI dataset is available at http://www.esa-oceancolour-cci.org. First, MODIS-Aqua Level-3 mapped data of Rrs (for wavelengths 412, 443, 488, 531, 547, 667, and 678 nm) were acquired at a spatial resolution of 4 km, and an 8-day temporal resolution, for the Red Sea, covering a 15-year period spanning from 2003 to 2017. Secondly, we used Level-2 MERIS-derived Rrs data (for wavelengths 413, 443, 490, 510, 560, 620, 665, 681, and 709 nm) at a 1.2 km and 1-day resolution for a 9-year period (2002–2010), covering the region of Al-Lith, Saudi Arabia. The region of Al-Lith and its aquaculture facility, is located between 19◦12’0”N and 20◦6’0”N latitude and 40◦0’0”E and 42◦0’0”E longitude (see red box in Figure1). Previous studies have suggested that the aforementioned region is subject to the substantial nutrient loading from NAQUA aquaculture Remote Sens. 2020, 12, 3695 3 of 14 effluents [11,20,21]. Finally, version 4.1 of the ESA OC-CCI product was used. This product is comprised of merged and bias-corrected Chl-a data from MERIS, MODIS, Sea-Viewing Wide Field-of-View Sensor (SeaWiFS), and the Visible Infrared Imaging Radiometer Suite (VIIRS) satellite sensors. Level-3 mapped data of Chl-a were obtained at 4 km spatial resolution and 8-day temporal resolution for the period 2002 to 2010 in the Al-Lith region. We note that standard remote sensing algorithms may systematically overestimate Chl-a when compared with in situ measurements in the Red Sea. This is mainly due to excess chromophoric dissolved organic matter (CDOM) absorption per unit chlorophyll in this basin when compared with average global conditions [22]. However, Brewin et al. [23] and Racault et al. [24] have demonstrated that the OC-CCI derived Chl-a dataset exhibits a good agreement with independent in situ Chl-a datasets in coastal and open waters of the Red Sea. In addition, several studies have suggested that the OC-CCI product is characterized by higher data availability in comparison to single-sensor-based missions [24–26]. Thus, we are confident in using the OC-CCI derived Chl-a dataset for investigating interactions between HABs and local aquaculture in the coastal watersRemote Sens. of Al-Lith. 2020, 12, x FOR PEER REVIEW 4 of 14

Figure 1. Map showing the bathymetry of the Red Sea (acquired from the General Bathymetric Chart of Figure 1. Map showing the bathymetry of the Red Sea (acquired from the General Bathymetric Chart the Oceans (GEBCO_2014 Grid, version 20150318, http://www.gebco.net/)). The Red Sea is divided into of the Oceans (GEBCO_2014 Grid, version 20150318, http://www.gebco.net/)). The Red Sea is divided four different provinces, following Raitsos et al. (2013): the Northern Red Sea (NRS), North-Central Redinto Sea four (NCRS), different South-Central provinces, Redfollowing Sea (SCRS) Raitsos and et Southern al. (2013): Red the Sea Northern (SRS). We Red also Sea note (NRS), that the North- red boxCentral indicates Red theSea geographical(NCRS), South-Central location of theRed Al-Lith Sea (SCRS) region, and Saudi Southern Arabia. Red Sea (SRS). We also note that the red box indicates the geographical location of the Al-Lith region, Saudi Arabia.

3. Results

3.1. Atlas of HABs in the Red Sea We produced a high-resolution atlas of HAB events to depict their overall spatial variability in the Red Sea. Throughout the 15-year period (2003–2017), the eastern coast of the Red Sea (excluding the NRS) hosts the highest number of HAB events, whilst more persistent events can be observed in a substantial part of the SRS (Figure 2a,b). Large-scale events were apparent along the western coast and open waters of the SCRS and the SRS (Figure 2c). Additionally, Red Sea HABs exhibit a notable seasonality in terms of the total number of events, with most HABs occurring during summer (at least 30 events), and fewer events occurring during winter and autumn (at least 21 events) (Figure 3). In general, we observed the highest number of HAB events in the SRS, followed by the SCRS and then the NCRS (Figure 2). HAB events in the Red Sea appear to decrease northward and no events were detected by the remote sensing algorithm in the NRS over the study period (Figure 2). Next, we provide spatial and seasonal descriptions of HAB events for the three Red Sea provinces where HABs were detected.

Remote Sens. 2020, 12, 3695 4 of 14

2.2. Aquaculture Production Dataset Aquaculture production data were acquired from the Sea Around Us project (http://www. seaaroundus.org) for examining the possible linkages between aquaculture and HABs. The Sea Around Us project is based on a global analysis that aims to generate a database of the annual reported aquaculture production in all maritime countries from 1950 to 2010 [27–29]. The project has also documented the annual mariculture production for countries bordering the Red Sea, including Egypt, Sudan, Eritrea, , Saudi Arabia, Jordan, and Israel. The average annual production of NAQUA, the largest shrimp farming aquaculture facility in the Red Sea, was reported by this project for the period spanning 1985 to 2010 [27–29]. Here, we utilized the average annual production dataset of the NAQUA aquaculture facility for the period 2002 to 2010, corresponding with the available MERIS derived Rrs observations. We note that the aquaculture production dataset was obtained from a report submitted by the Kingdom of Saudi Arabia to the Food and Agricultural Organization (FAO) of the United Nations (http://www.fao.org/fishery/countrysector/naso_saudiarabia/en).

2.3. Approach Our approach is comprised of two parts: (1) Produce an atlas of HAB events in the Red Sea, and (2) Investigate the interactions between HABs and aquaculture. For the first aim, we implemented the remote sensing algorithm developed recently by Gokul et al. [17] on a 15-year MODIS-derived Rrs dataset (2003–2017) to reveal spatial patterns in HAB frequency, duration, and spatial coverage. We also evaluated the temporal patterns of HABs in terms of the total number of events in the Red Sea over three main seasons (winter (January to April), summer (May to August), and autumn (September to December). In order to provide a more comprehensive spatial and temporal description of HAB events, we divided the Red Sea into four regions following Raitsos et al. [30]: the Northern Red Sea (NRS; 25.5–30◦ N), the North-Central Red Sea (NCRS; 22–25.5◦ N), the South-Central Red Sea (SCRS; 17.5–22◦ N), and the Southern Red Sea (SRS; 12.5–17.5◦ N) (Figure1). For the second part of our analysis, we applied the algorithm to MERIS-derived Rrs in the Al-Lith region over a 9-year period (2002–2010), in order to examine the possible links between HAB events and the largest aquaculture facility in the Red Sea. In addition, satellite-derived Chl-a concentrations (OC-CCI) were analysed in the coastal waters of Al-Lith over the period 2002 to 2010, in order to study the potential links between the aquaculture facility and HABs.

3. Results

3.1. Atlas of HABs in the Red Sea We produced a high-resolution atlas of HAB events to depict their overall spatial variability in the Red Sea. Throughout the 15-year period (2003–2017), the eastern coast of the Red Sea (excluding the NRS) hosts the highest number of HAB events, whilst more persistent events can be observed in a substantial part of the SRS (Figure2a,b). Large-scale events were apparent along the western coast and open waters of the SCRS and the SRS (Figure2c). Additionally, Red Sea HABs exhibit a notable seasonality in terms of the total number of events, with most HABs occurring during summer (at least 30 events), and fewer events occurring during winter and autumn (at least 21 events) (Figure3). In general, we observed the highest number of HAB events in the SRS, followed by the SCRS and then the NCRS (Figure2). HAB events in the Red Sea appear to decrease northward and no events were detected by the remote sensing algorithm in the NRS over the study period (Figure2). Next, we provide spatial and seasonal descriptions of HAB events for the three Red Sea provinces where HABs were detected. Remote Sens. 2020, 12, x FOR PEER REVIEW 5 of 14

3.1.1. North-Central Red Sea The western coast of the NCRS experienced a small number of HAB events over the study period (at least three events, Figure 2a), which were generally of short duration (less than nine days, Figure 2b) and low spatial coverage (less than 500 km2, Figure 2c). Most of the east coast experienced fewer events, apart from the southern part of the NCRS, where the highest number of events (at least 16) were recorded. HABs along the east coast exhibit a longer duration in comparison to the west coast, ranging from 9 to 16 days and a mean spatial coverage ranging from 500 to 5000 km2. The seasonality of HAB events was investigated in the NCRS and is presented in Figure 3a–c. Overall, we observed the highest number of HAB events (at least 12 events) during summer and fewer events during winter and autumn (at least 3 events). Over the 15-year period, no HAB events were detected on the western coastline of the NCRS region during winter and autumn, while a small number of events were observed during summer (at least three events). On the eastern coast, the total number of HAB events was at least 12 in the southern part of NCRS and decreased towards the northern part of the region Remote Sens. 2020, 12, 3695 5 of 14 to at least 3 events during summer (Figure 3b).

Remote Sens. 2020, 12, x FOR PEER REVIEW 6 of 14 maximum HAB events was observed during summer (at least 12 events). In contrast, we observed the largest number of HAB events along the western coast of SCRS during autumn (at least nine events) while relatively fewer events over winter and summer seasons (at least six events).

3.1.3. Southern Red Sea The SRS exhibited a higher occurrence of HABs than anywhere else in the Red Sea (reaching at least 24 events), which were characterized by a longer duration and higher spatial coverage. The eastern coastline of the SRS region experienced the highest number of HAB events (at least 18), while fewer events occurred on the west coast and the open waters of the region (Figure 2a). A substantial part of the SRS was observed to have more long-lasting events (17–32 days, Figure 2b). The mean spatial coverage on the east coast was mostly low (500 km2 or less), whilst the southern part of the SRS had spatial coverage ranging from 500–5000 km2. The mean spatial coverage of HAB events reached values as high as ~42,904 km2 in the open waters of the SRS (Figure 2c). The seasonal investigation of the SRS revealed that the region is subjected to fewer events during summer (at least Figure 2. Atlas of harmful algal blooms (HAB) events over the Red Sea during 2003–2017. The maps Figure 2. Atlas of harmful algal blooms (HAB) events over the Red Sea during 2003–2017. The maps six events).represent: The total (a) the number total number of HAB of HAB events events, in (theb) the SRS average was durationhigher during of HAB winter events, and(at (leastc) the 12 average events) represent: (a) the total number of HAB events, (b) the average duration of HAB events, and (c) the than autumnspatial coverage(at least 9 of events) HAB events. (Figure 3a–c). average spatial coverage of HAB events.

3.1.2. South-Central Red Sea In the SCRS, the majority of the HAB events were detected over the eastern coastline, while fewer events were observed along the western coast and open waters of the region (Figure 2a). The duration of HAB events appeared to be considerably higher along the eastern coastline and open waters (9–16 days), in comparison to the western coast, which exhibited shorter events (less than 9 days) (Figure 2b). On the east coastline, the mean spatial coverage is less than 500 km2 in the northern part of SCRS and increases towards the southern part of the region at least ~5000 km2. Noticeably higher spatial coverage was observed over the western coast and the open waters of the region (>5000 km2) (Figure 2c). Overall, the total number of HABs was highest during summer in the SCRS region (at least 12 events), followed by autumn (at least 9 events) and a moderately low number of events during winter (at least 6 events) (Figure 3a–c). Throughout the 15-year study, a small number of events (at least three events) were detected in the open waters of SCRS during summer, whilst no HAB events were observed in the open waters during winter and autumn (Figure 3a–c). The eastern coastline of the SCRS experienced few events during the winter and autumn (at least 6 events), while

Figure 3. Seasonal occurrence of the number of HAB events for the period 2003–2017. The maps Figure 3. Seasonal occurrence of the number of HAB events for the period 2003–2017. The maps represent: (a) Winter climatology (January to April), (b) Summer climatology (May–August), represent: (a) Winter climatology (January to April), (b) Summer climatology (May–August), and (c) and (c) Autumn climatology (September–December). Autumn climatology (September–December). 3.1.1. North-Central Red Sea Overall, our atlas reveals that regions along the east coast of the Red Sea (excluding the NRS) appearThe to be western areas coastof higher of the risk NCRS of experiencedoccurrence of a smallHABs. number The SCRS of HAB and events SRS exhibit over the the study highest period numbers(at least of three HABs events, on the Figure eastern2a), coastline which were (reaching generally at least of short 18 events), duration as (less well than as persistent nine days, and Figure fairly2b) 2 widespreadand low spatial events coverage (at least ~5000 (less thankm2). 500 It is km worthwhile, Figure2 c).to note Most that of themost east of coastthe HAB experienced events on fewer the eastevents, coast apartof the fromSCRS the region southern were observed part of the during NCRS, summer where (Figure the highest 3b). numberIn the following of events Section, (at least we 16) were recorded. HABs along the east coast exhibit a longer duration in comparison to the west coast, utilize the available MERIS derived Rrs observations (2002–2010) to examine the possible linkages between HABs in the SCRS and the local aquaculture facility.

3.2. Interactions of HABs with Aquaculture In this Section, we investigated the possible interactions between HABs in the Al-Lith and the nearby NAQUA aquaculture facility between 2002–2010 (see Data and methods). First, we compared the spatial coverage of HAB events (in km2) in the coastal waters of Al-Lith during the summer season

Remote Sens. 2020, 12, 3695 6 of 14 ranging from 9 to 16 days and a mean spatial coverage ranging from 500 to 5000 km2. The seasonality of HAB events was investigated in the NCRS and is presented in Figure3a–c. Overall, we observed the highest number of HAB events (at least 12 events) during summer and fewer events during winter and autumn (at least 3 events). Over the 15-year period, no HAB events were detected on the western coastline of the NCRS region during winter and autumn, while a small number of events were observed during summer (at least three events). On the eastern coast, the total number of HAB events was at least 12 in the southern part of NCRS and decreased towards the northern part of the region to at least 3 events during summer (Figure3b).

3.1.2. South-Central Red Sea In the SCRS, the majority of the HAB events were detected over the eastern coastline, while fewer events were observed along the western coast and open waters of the region (Figure2a). The duration of HAB events appeared to be considerably higher along the eastern coastline and open waters (9–16 days), in comparison to the western coast, which exhibited shorter events (less than 9 days) (Figure2b). On the east coastline, the mean spatial coverage is less than 500 km 2 in the northern part of SCRS and increases towards the southern part of the region at least ~5000 km2. Noticeably higher spatial coverage was observed over the western coast and the open waters of the region (>5000 km2) (Figure2c). Overall, the total number of HABs was highest during summer in the SCRS region (at least 12 events), followed by autumn (at least 9 events) and a moderately low number of events during winter (at least 6 events) (Figure3a–c). Throughout the 15-year study, a small number of events (at least three events) were detected in the open waters of SCRS during summer, whilst no HAB events were observed in the open waters during winter and autumn (Figure3a–c). The eastern coastline of the SCRS experienced few events during the winter and autumn (at least 6 events), while maximum HAB events was observed during summer (at least 12 events). In contrast, we observed the largest number of HAB events along the western coast of SCRS during autumn (at least nine events) while relatively fewer events over winter and summer seasons (at least six events).

3.1.3. Southern Red Sea The SRS exhibited a higher occurrence of HABs than anywhere else in the Red Sea (reaching at least 24 events), which were characterized by a longer duration and higher spatial coverage. The eastern coastline of the SRS region experienced the highest number of HAB events (at least 18), while fewer events occurred on the west coast and the open waters of the region (Figure2a). A substantial part of the SRS was observed to have more long-lasting events (17–32 days, Figure2b). The mean spatial coverage on the east coast was mostly low (500 km2 or less), whilst the southern part of the SRS had spatial coverage ranging from 500–5000 km2. The mean spatial coverage of HAB events reached values as high as ~42,904 km2 in the open waters of the SRS (Figure2c). The seasonal investigation of the SRS revealed that the region is subjected to fewer events during summer (at least six events). The total number of HAB events in the SRS was higher during winter (at least 12 events) than autumn (at least 9 events) (Figure3a–c). Overall, our atlas reveals that regions along the east coast of the Red Sea (excluding the NRS) appear to be areas of higher risk of occurrence of HABs. The SCRS and SRS exhibit the highest numbers of HABs on the eastern coastline (reaching at least 18 events), as well as persistent and fairly widespread events (at least ~5000 km2). It is worthwhile to note that most of the HAB events on the east coast of the SCRS region were observed during summer (Figure3b). In the following Section, we utilize the available MERIS derived Rrs observations (2002–2010) to examine the possible linkages between HABs in the SCRS and the local aquaculture facility.

3.2. Interactions of HABs with Aquaculture In this Section, we investigated the possible interactions between HABs in the Al-Lith and the nearby NAQUA aquaculture facility between 2002–2010 (see Data and methods). First, we compared Remote Sens. 2020, 12, 3695 7 of 14

Remote Sens. 2020, 12, x FOR PEER REVIEW 7 of 14 the spatial coverage of HAB events (in km2) in the coastal waters of Al-Lith during the summer seasonand the and average the average annual annual production production (in tonnes) (in tonnes) from the from shrimp the shrimp farming farming aquaculture aquaculture facility facility(Figure (Figure4b). In4 general,b). In general, the spatial the spatial coverage coverage of HAB of even HABts events in thein Al-Lith the Al-Lith region region during during summer summer was found was foundto increase to increase in conjunction in conjunction with the with local the aquaculture local aquaculture production production over the over period the period2002–2010 2002–2010 (Figure 2 (Figure4b). Before4b). Before 2005, the 2005, spatial the spatial coverage coverage of HABs of HABs was waslow low(on (onaverage average 65 km 65 km2) near) near the theaquaculture aquaculture site siteover over the thesummer summer season, season, coinciding coinciding with with fairly fairly low levels low levels of annual of annual aquaculture aquaculture production production (~4000 (~4000tonnes). tonnes). Following Following 2005, the 2005, spatial the spatial coverage coverage with withthe presence the presence of HABs of HABs rapidly rapidly increased increased and 2 andreached reached a maximum a maximum of of392 392 km km2 byby 2010, 2010, corresponding corresponding with with the the highest productionproduction ofof locallocal 1 aquacultureaquaculture (22,370(22,370 tonnes tonnes year year−−1).). In orderorder toto furtherfurther examineexamine thethe presencepresence ofof HABsHABs inin Al-Lith Al-Lith coastalcoastal waters waters over over the the summer summer season, season, we we presented presented a a seasonal seasonal time time series series of of satellite-derived satellite-derivedChl-a Chl- concentrationsa concentrations (as a(as proxy a proxy of nutrient of nutrient concentrations) concentrations) over threeover dithreefferent different seasons seasons in the coastal in the waterscoastal ofwaters Al-Lith of duringAl-Lith 2002–2010during 2002–2010 (see Data (see and Data Methods). and Methods). During During summer, summer,Chl-a concentrations Chl-a concentrations were 3 higherwere higher (>1 mg (>1 m mg− ), m in−3), comparison in comparison to winter to winter and and autumn autumn over over the the nine-year nine-year period. period. In In addition, addition, wewe noticed noticed that that summer summerChl-a Chl-aconcentrations concentrations exhibit exhibit a consistent a consistent increase increase over over the period the period of 2002–2010 of 2002– in2010 the in coastal the coastal waters waters of Al-Lith of Al-Lith (Figure (Figure4c). 4c).

Figure 4. (a) Map showing the location of aquaculture facility in Al-Lith along the east coast of the Red Figure 4. (a) Map showing the location of aquaculture facility in Al-Lith along the east coast of the Sea. (b) Relationship between the spatial coverage of MERIS-derived HABs (in km2) in the Al-Lith Red Sea. (b) Relationship between the spatial coverage of MERIS-derived HABs (in km2) in the Al- region and the average annual production (in tonnes) of Al-Lith’s aquaculture facility over the period Lith region and the average annual production (in tonnes) of Al-Lith’s aquaculture facility over the between 2002 and 2010. (c) Seasonal time series of satellite-derived Chl-a in the coastal waters of Al-Lith period between 2002 and 2010. (c) Seasonal time series of satellite-derived Chl-a in the coastal waters over the period 2002 to 2010. The Chl-a dataset was acquired from version 4.1 of the ESA OC-CCI of Al-Lith over the period 2002 to 2010. The Chl-a dataset was acquired from version 4.1 of the ESA product and the annual aquaculture production dataset was obtained from the Sea Around Us project OC-CCI product and the annual aquaculture production dataset was obtained from the Sea Around (http://www.seaaroundus.org/). Us project (http://www.seaaroundus.org/). 4. Discussion 4. Discussion Over the past few decades, HABs have adversely affected coastal ecosystem services in the Red Sea, includingOver the past fisheries, few decades, aquaculture, HABs and have tourism adversely [8– 17affected]. However, coastal priorecosystem to this services study, in research the Red dedicatedSea, including to the , investigation aquaculture, of HAB spatiotemporaland tourism [8–17]. variability However, and interactions prior to this with study, aquaculture research industriesdedicated remained to the investigation limited. Our of studyHAB spatiotemporal demonstrated that variability the remote and sensinginteractions algorithm with aquaculture developed byindustries Gokul et remained al. [17] provides limited. a Ou cost-er studyffective demonstrated and valuable that tool the for remote (1) producing sensing algorithm an atlas of developed HABs to characterizeby Gokul et theiral. [17] spatial provides patterns a cost-effective and seasonal and variability valuable tool in the for Red (1) Sea,producing and (2) an investigating atlas of HABs the to linkagescharacterize between their HABs spatial and patterns the largest and aquacultureseasonal variability facility inin the the region. Red Sea, and (2) investigating the linkagesFirst, between we discuss HABs the and possible the largest oceanographic aquaculture mechanisms facility in thatthe region. could potentially facilitate HAB eventsFirst, in the we Red discuss Sea. Ourthe possible atlas reveals oceanographic that the highest mechanisms number that of HAB could events potentially occurred facilitate in the SRS,HAB followedevents in by the the Red SCRS Sea. andOur subsequently atlas reveals that the NCRS,the highest over number the period of HAB of 2003–2017. events occurred The SRS in andthe SRS, the substantialfollowed by parts the of SCRS SCRS and are subsequently subject to a biannual the NCRS influx, over of nutrient-rich the period of waters 2003–2017. from the The Indian SRS and Ocean the throughsubstantial the Gulfparts of of Aden, SCRS driven are subject by the seasonallyto a biannual reversing influx Indian of nutrient-rich monsoon winds waters [25 ,from31–39 the]. During Indian Ocean through the Gulf of Aden, driven by the seasonally reversing Indian monsoon winds [25,31– 39]. During the winter monsoon (October–April), prevailing south-easterly winds promote the northward advection of nutrient-rich surface waters into the Red Sea from the Gulf of Aden [32,40– 42]. During the summer monsoon (May–September), prevailing winds reverse their direction,

Remote Sens. 2020, 12, 3695 8 of 14 the winter monsoon (October–April), prevailing south-easterly winds promote the northward advection of nutrient-rich surface waters into the Red Sea from the Gulf of Aden [32,40–42]. During the summer monsoon (May–September), prevailing winds reverse their direction, causing intense in the Gulf of Aden, ultimately generating an influx of nutrient-rich water through an intermediate water layer (Gulf of Aden Intermediate Water—GAIW) into the shallow waters of SRS [36]. This influx of nutrient-rich waters during both monsoons could disseminate HABs in parts of the SRS and SCRS regions throughout the year [12–14,17,18]. Besides the influx of nutrient-rich waters from the Indian Ocean into the Red Sea, the discharge of large quantities of nutrients from domestic, industrial, and agricultural wastes may also facilitate the growth of HAB species in the SRS and SCRS regions [8,9,11,18,20,21]. For instance, Alkershi and Menon [9] documented a dinoflagellate HAB event along the coastal waters of Yemen during March 2009. The high density of this dinoflagellate bloom (up to 5.5 105 cells L 1) was observed at a station where large amounts of remains of slaughtered × − fishes and waste from fishing boats are discharged. We also note that HAB events in the Red Sea region were found to decrease northward and no events were detected by the remote sensing algorithm in the NRS over the study period. In addition, previous studies demonstrated that HABs in the NRS were 4 1 often observed at low cell densities (<1 10 cells L− ), corresponding to low Chl-a concentrations 3 × (<1 mg m− )[18,43–45]. For instance, Madkour et al. [44] reported a cyanobacteria bloom (up to 7 103 cells L 1) that was associated with Chl-a concentrations up to 0.9 mg m 3, which also co-occurred × − − with along the Egyptian coast of the NRS between 2007–2008. However, the remote sensing algorithm used in this analysis is only capable of detecting the presence of a HAB event when Chl-a concentrations and cell abundances exceed a minimum value of ~1 mg m 3 and ~1 104 cells L 1, − × − respectively [17]. We thus note that the HAB events were not detected by the remote sensing algorithm in the NRS region over the 15-year period from 2003 to 2017. A more detailed discussion of the possible oceanographic mechanisms that were responsible for the majority of HAB outbreaks in the three provinces of the Red Sea is narrated below. In the NCRS, HABs were more frequent on the south-eastern coast of the region and some of these events were found to be consistent with the concurrent in situ sampling locations. For instance, the presence of a HAB event detected by the remote sensing algorithm is in good agreement with the study of Catania et al. [16], who documented the occurrence of the benthic dinoflagellate Ostreopsis sp. over the region of Thuwal (Saudi Arabia) during the summer of 2013 (Figure S1). Catania et al. [16] also revealed that HAB events occurred off the coast of Thuwal (Saudi Arabia) during the summer monsoon, when warm caused corals to bleach on the inshore reefs. The corals on these inshore reefs appeared to suffer high mortality rates and the increased availability of dead coral surfaces could have favored the proliferation of HABs in this region [16]. In addition, we detected a HAB event that was found to concur with Touliabah et al. [46], who reported a cyanobacteria bloom event in the south-eastern coast of NCRS () during the summer of 2004 (Figure S1). This bloom event was linked to the nutrient-rich domestic wastewater discharge along the coastal waters of Jeddah [46]. Our results also suggest a summer peak (in particular during May) in the time series of satellite-derived Chl-a concentration (a proxy for high nutrient concentration) during 2004 over the region of Jeddah, where the HAB event was detected (Figure S2). In the SCRS, we observed the highest number of HAB events along the eastern coast of the region, and the majority of those events occurred during summer. This is also concurrent with several previous studies [8,10,11,18,20] that reported HAB events along the east coast of SCRS in the coastal waters of Al-Lith, Doga, and Jizan during summer. The remotely sensed HAB events were found to coincide with in situ observations acquired during previous campaigns [8,11] in Al-Lith and Doga during the summers of 2010 and 2004, respectively (Figure S1). The prevailing north-westerly wind patterns observed during summer 2010 (Al-Lith) and 2004 (Doga) (see Figure S1) may transport HABs towards the south along the east coast of SCRS [8]. While HABs were detected over large distances in the east coastal waters of SCRS, they mainly occurred locally, probably as a result of anthropogenic nutrients and waste produced from Al-Lith’s aquaculture facility [8,10,11,18,20]. Kurten et al. [20] suggested Remote Sens. 2020, 12, 3695 9 of 14 that the supply of dissolved and particulate organic matter from aquaculture effluents could lead to excessive nutrient loading that may disseminate HABs along the east coast of the SCRS during the summer monsoon. The time series of Chl-a concentration acquired in Al-Lith and Doga (east-coast of 3 SCRS) during 2010, and 2004, respectively revealed that elevated Chl-a values (>1 mg m− ; a proxy for high nutrient concentration) were observed over summer season (see Figure S2). Few studies have been conducted on the distribution and abundance of HABs in the western coastline of SCRS (in particular Sudanese Red Sea coasts) [47,48]. For example, El Hag and Nasir [47] recorded high cell densities (up to 1 105 cells L 1) of harmful dinoflagellates along the coastal waters of Sudan. × − This high accumulation of HABs along the Sudan coastal waters was associated with the high nutrient loadings from the economical and industrial developments on the Sudanese Red Sea coast [49,50]. Previous studies investigated the circulation dynamics, including surface currents and mesoscale eddies, which may increase the availability of nutrients and occupy large areas in the open waters of the SCRS region [30,51]. These high nutrients could be responsible for the large-scale HAB events in the western coastline and open waters of the SCRS region [18,47,48]. The SRS has been subjected to more HAB events than anywhere else in the Red Sea, showing the most persistent and large-scale events in comparison to the SCRS and NCRS. Previous research has also observed HABs in the SRS (in particular the coastal waters of Yemen) over the last two decades [9,12–14,17]. We detected the presence of a HAB event in the coastal waters of Al-Hodeidah during winter 2009, which is consistent with the results of Alkershi and Menon [9] who documented a bloom of N. scintillans/miliaris during the winter 2009 in the coastal waters of Al-Hodeidah (Yemen) [see Figure S1]. Large quantities of nutrients were observed in the coastal waters of Al-Hodeidah after the remains of slaughtered fishes and waste from fishing boats were discharged in March 2009 [9]. The time series analysis over Al-Hodiedah (Yemeni coastal waters) also confirmed that elevated Chl-a 3 values (>1 mg m− ; a proxy for high nutrient concentration) were observed between February–March in 2009 (see Figure S2). Furthermore, south-easterly winds were clearly observed during winter 2009 over the SRS, which could have re-distributed HAB species to the open waters of the region (Figure S1). To support this observation, Gokul et al. [17] suggested that regional dynamic circulation could transfer HABs hundreds of kilometers away. In addition, our results are consistent with Alkwari et al. [14], who reported the occurrence of intense P. bahamense blooms (<1 105 cells L 1) along the coastal waters × − of Yemen during winter 2013 (see Station ‘S20 in the HAB map of Al-Hodeidah region (winter 2013) in Figure S1). Besides, Alkawari et al., [14] reported a cyanobacteria T. erythraeum blooms that were observed as spatially less dense (>1 104 cells L 1) along with the dinoflagellates P. bahamense in the × − coastal waters of Yemen during winter 2013. These HAB events were linked to south-easterly wind patterns that promotes the northward advection of nutrient-rich surface waters into the Red Sea from the Gulf of Aden during the winter monsoon [14,18]. However, the remote sensing algorithm of Gokul et al. [17] is limited at detecting the cyanobacteria T. erythraeum along the coastal waters of Yemen during winter 2013 (see Station “S1” in the HAB map of Al-Hodeidah region (winter 2013) in Figure S1). We therefore acknowledge an uncertainty in the accuracy of the remote sensing model at detecting HABs that are spatially less dense, and/or composed of mixed assemblages of phytoplankton (especially cyanobacteria with dinoflagellates). We also note that the persistent presence of clouds, sun-glint, and sensor saturation over sand severely reduces the retrieval of satellite ocean color observations from the MODIS-Aqua data in the southern part of the Red Sea region (including SCRS) during the summer monsoon (June–September) [23–25,52,53]. This may inhibit the investigation of HABs in the region during the aforementioned period and thus could explain why we observed relatively few events in the SRS during summer (see Figure3b). The satellite observations that are a ffected by the adverse atmospheric condition (Haze and clouds) may cause an uncertainty in determining the duration of HAB events over the summer monsoon. For example, Mohamed and Al-Shehri [11] reported the occurrence of a HAB event ( H. akashiwo) between mid-May and mid-June (24–32 days) of 2010 in the vicinity of Al-Lith’s aquaculture facility. However, these adverse atmospheric conditions may hinder the ability of the remote sensing algorithm of Gokul et al. [17] to detect the aforementioned Remote Sens. 2020, 12, 3695 10 of 14

HAB event during June 2010. We therefore note that the duration of remotely sensed HAB events was found to be considerably lower in the Al-Lith region (9–16 days) during 2010, in comparison to the in situ observations. HABs occur naturally in the Red Sea but may also be exacerbated with anthropogenically-driven activities such as pollution, local aquaculture expansion and ballast water transport [8–11,18,20,21]. The NAQUA is the largest aquaculture facility in the Red Sea, is an important contributor to the socio-economic development of the Kingdom of Saudi Arabia and helps to meet the growing demand of seafood products in the nation [21,54–57]. Although NAQUA is important for food and economic prosperity, it is a point source of anthropogenic nutrients to the coastal waters of Al-Lith [10,11,18,21,56]. A recent study suggested that the highest discharge of nutrients and waste follows the flushing of shrimp aquaculture in the coastal waters of Al-Lith [21]. The aquaculture facility aims for three harvests per year and after each harvest, the ponds are flushed and dried for one month. The exact timing of flushing is unknown, although the harvest cycles suggest that the flushing of the aquaculture ponds takes place all year round [21]. Furthermore, the wastewater discharged from the aquaculture outfall may facilitate the proliferation of HAB species in an otherwise oligotrophic region during the stratified conditions in summer [10,11,20,21,30]. We found that the spatial coverage of HABs in regions nearby to NAQUA increased in conjunction with the average annual aquaculture production during the nine-year period (2002–2010) (Figure4b). In addition, we noticed that satellite-derived Chl-a 3 concentrations were also high (>1 mg m− ) during the summer season and exhibited an increasing trend over the period of 2002–2010 (Figure4c). This is analogous with the results of Hozumi et al. [21], who revealed that water discharged from the aquaculture facility was characterized by high in situ 3 Chl-a concentration (>1 mg m− ) during the summer season between 2014 and 2015. Thus, our results imply that HAB events have expanded both in time and space alongside intensified aquaculture production in the coastal regions of Al-Lith. Mohamed and Al-Shehri [11] also suggested that the intensive aquaculture operations of the NAQUA facility causes self-pollution as a result of excessive feeding and fish feces, causing in the aquaculture area. This may disseminate HABs in the coastal waters of Al-Lith over summer monsoon. These HAB events may pose a serious threat to the sustainable exploitation of the aquaculture sector [11,21]. Thus, the expansion and sustainability of Al-Lith’s aquaculture facility are dependent on the adoption of management practices that minimize the impact of excessive nutrient loading. For instance, as a part of the sustainability programme, Al-Lith’s NAQUA facility is developing plantations in order to mitigate the environmental issues including impacts on public health, fisheries, and aquaculture (https://thefishsite.com/articles/ sustainable-antibiotic-free-aquaculture-on-the-desert-coast). However, further efforts should be made in managing the aquaculture wastewaters, since there is a clear association between the excessive nutrient loading from aquacultures and increased phytoplankton biomass (including harmful ). From a management perspective, HABs in the Red Sea are considered to be one of the most important direct drivers of biodiversity loss and change in ecosystem services regionally [13,16,18]. As we have shown, our atlas can identify high-risk areas in the Red Sea. For instance, we have detected a potential high-risk area in the NCRS (particularly along the southeastern coastline). As this region supports an important level of biodiversity and may consequently sustain numerous communities of organisms throughout the Red Sea [38,58,59], we suggest that the NCRS may possibly require HAB management. In comparison to the NCRS, the SCRS has experienced a higher occurrence of HABs along its’ eastern coast over the last two decades. This region is well known for its annual whale shark aggregations [21,60,61], yet shows an accumulation of HAB threats. Thus, there is a pressing need to conduct further research in this region in order to elucidate the potential detrimental impacts of HABs on marine organisms. We also highlight the possible need for HAB management in Red Sea regions other than the southern part, such as the central part of the basin, as these regions are subject to the substantial elevation of nutrient loading associated with the coastal urbanization, industrial expansion and aquaculture development along the Saudi Arabian Red Sea coast [8,10,11,18,20,46]. We also propose the SRS to be a prime candidate, as it exhibits the highest number of HABs as well Remote Sens. 2020, 12, 3695 11 of 14 as the most persistent and large-scale events in the entire Red Sea. In addition, it is also a region where the seasonal inflow of surface water from the Gulf of Aden appears to play an important role in the maintenance of pelagic organisms and their distribution within the Red Sea [12–14,30,39,62,63]. Previous studies have also identified the region as the most highly HAB-affected part of the Red Sea and is often associated with severe fish mortalities and numerous ecological impacts [9,12–14,17].

5. Conclusions Our results revealed that the highest number of HAB events occurred in the SRS, followed by the SCRS and the NCRS. In addition, HAB events detected in the SRS and SCRS were characterized by a longer duration and an increased spatial extent, in comparison to the NCRS. In particular, regions along the east coast (excluding the NRS) appear to be more at high-risk for the occurrence of HABs. HAB events exhibit a distinct seasonality, with a higher number of events occurring during summer in comparison to winter and autumn. Investigations of the potential linkages of HABs with the largest aquaculture facility in the Red Sea revealed that HABs have expanded, both in space and time, over the east coast of the SCRS in conjunction with intensified local aquaculture production. It is therefore possible that HAB events in this region have increased alongside farming operations, which could pose a serious threat to the sustainable exploitation of the aquaculture sector and the coastal environment. The implementation of integrated, conservation-oriented management plans are necessary if HABs become more frequent in the proximity of the aquaculture facility. Since the aquaculture industry is a financial asset for the Kingdom of Saudi Arabia, a national wastewater management program should also be implemented, in order to prevent the excessive nutrient loading into the oligotrophic Red Sea ecosystem.

Supplementary Materials: The following are available online at http://www.mdpi.com/2072-4292/12/22/3695/s1, Figure S1: Remotely sensed HAB events and the wind speed (m/s) patterns over the regions where the in situ sampling was conducted in the Red Sea during the different periods from 2003 to 2017, Figure S2: Time series analysis of satellite-derived Chl-a over the regions where the in situ sampling was conducted in the Red Sea during the different periods from 2003 to 2017, Figure S3: Remotely sensing HAB event in the Al-lith aquaculture facility, Figure S4: Remotely sensing HAB event in the Al-lith aquaculture facility, Table S1: Summary of the (HAB) species reported by the various studies in the Red Sea waters. Author Contributions: Conceptualization: E.A.G., D.E.R. and I.H.; methodology: E.A.G. and D.E.R.; software: E.A.G.; validation: E.A.G.; formal analysis: E.A.G. and D.E.R.; writing—original draft preparation: E.A.G.; writing—review and editing: E.A.G., D.E.R., J.A.G. and I.H.; data curation: E.A.G.; supervision, D.E.R. and I.H.; project administration: I.H.; funding acquisition: I.H. All authors have read and agreed to the published version of the manuscript. Funding: This research was funded by the King Abdullah University of Science and Technology (KAUST) Office of sponsored Research (OSR) under the Virtual Red Sea Initiative (Grant # REP/1/3268-01-01). Acknowledgments: The authors are grateful to the Ocean Biology Processing Group of NASA for the distribution of the MODIS-Aqua and MERIS datasets and the development and support of the SeaDAS software. The authors are also grateful to the ESA Ocean Colour CCI team for providing and processing the Chl-a dataset. We are also grateful to the Sea Around Us project for providing the annual aquaculture production dataset. Conflicts of Interest: The authors declare no conflict of interest.

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